Enhanced Neural Processing by Covert Attention only during Microsaccades Directed toward the Attended Stimulus

Abstract

Attention can be "covertly" directed without eye movements; yet, even during fixation, there are continuous microsaccades (MSs). In areas V4 and IT of macaques, we found that firing rates and stimulus representations were enhanced by attention but only following a MS toward the attended stimulus. The onset of neural attentional modulations was tightly coupled to the MS onset. The results reveal a major link between the effects of covert attention on cortical visual processing and the overt movement of the eyes.

Keywords: IT; V4; attention; firing rate; microsaccades; object decoding; oculomotor system; visual cortex.

Figure 1.. Direction of MSs Reflect the Locus of Attention

(A) Example vertical and horizontal eye traces during a trial. The rapid shifts in positions are MSs. (B) The MS directions from the example trial. (C) Example stimuli shown for the three stimulus locations. A cue directed attention to one of the locations. (D) The population-averaged MS direction probability plots of MonkeyM1 for the three attention positions indicated by the “Cue” label (for monkey M2, positions were in the opposite hemifield).

Figure 2.. Neural Enhancement Occurs Only with MSs Directed towards Attention Location

(A and B) Example spike rasters locked to onset of MS directed toward (A) or away from (B) cued stimulus (Att-in). The black line shows average eye speed. (C and D) Population data combined across monkeys. Analysis was restricted to MSs directed toward the attended position. (C) Normalized population-averaged V4 firing rate for attention on the RF (POS1) and outside of the RF (POS3). Shaded area indicates ±SE. (D) Attention modulation index (Att-in − Att-out / Att-in + Att-out) (n = 253) computed 100–200 ms after MS onset. (E and F) Same analysis as in (C) and (D), but for MSs directed away from the attention position (i.e., toward the fixation target).

Figure 3.. V4 Control Data with Stimulus Jerked Toward or Away from the Fixation Point

(A) V4 population averaged V4 firing rate for stimulus jerked (by 0.3°) away from fixation (blue line and shading) or toward fixation (red line and shading). Shaded area indicates ±SE. After 300 ms, the stimulus was jerked back to the original position. (B) Firing rate modulation between jerk-toward and -away conditions (Jerk_toward − Jerk_away/Jerk_toward + Jerk_away) for each neuron for time windows of 50 ms to 150 ms after jerk time (transient response). The distribution did only slightly deviate from a distribution centered on zero. (C) Same as in (B), but for time windows of 150 ms to 250 ms after the jerk time. Distribution deviated more significantly with enhanced V4 firing rate for jerk away from fixation point.

Figure 4.. Onset of Attention Neural Effects Coupled to MS Onsets

(A) Normalized V4 spike rate and the averaged eye speed as a function of cue onset for stim-first sessions. Shaded area indicates ±SE. (B) The same as in (A), but trials were selected based on the timing of the MS occurrence toward the attended position. From top to bottom, the chosen selection time windows were: 50–150 ms, 200–300 ms, 250–350 ms, and 350–450 ms.

Figure 5.. Object Decoding Enhanced with MSs Directed towards Attention Location

(A) Schematic outline of the V4 and IT RFs in relation to the three stimulus locations. Stimuli presented in the V4 RF were decoded. (B) The 7 stimuli used. (C and D) V4 neurons. (C) Example neuron firing rates for two different stimuli (green line versus blue line) relative to the onset of MSs directed toward the attended location (left) or away from it (right). (D) Population-averaged decoding performance based on single-cell firing rates (100–200 ms after MS onset) using ANOVA as a function of MS direction and attention position. (E and F) The same as in (C) and (D), respectively, but for IT neurons.